Abstract

BackgroundSpecies with a restricted geographic distribution, and highly specialized habitat and dietary requirements, are particularly vulnerable to extinction. The Bale monkey (Chlorocebus djamdjamensis) is a little-known arboreal, bamboo-specialist primate endemic to the southern Ethiopian Highlands. While most Bale monkeys inhabit montane forests dominated by bamboo, some occupy forest fragments where bamboo is much less abundant. We used mitochondrial DNA (mtDNA) sequences to analyse the genetic structure and evolutionary history of Bale monkeys covering the majority of their remaining distribution range. We analysed 119 faecal samples from their two main habitats, continuous forest (CF) and fragmented forests (FF), and sequenced 735 bp of the hypervariable region I (HVI) of the control region. We added 12 orthologous sequences from congeneric vervets (C. pygerythrus) and grivets (C. aethiops) as well as animals identified as hybrids, previously collected in southern Ethiopia.ResultsWe found strong genetic differentiation (with no shared mtDNA haplotypes) between Bale monkey populations from CF and FF. Phylogenetic analyses revealed two distinct and highly diverged clades: a Bale monkey clade containing only Bale monkeys from CF and a green monkey clade where Bale monkeys from FF cluster with grivets and vervets. Analyses of demographic history revealed that Bale monkey populations (CF and FF) have had stable population sizes over an extended period, but have all recently experienced population declines.ConclusionsThe pronounced genetic structure and deep mtDNA divergence between Bale monkey populations inhabiting CF and FF are likely to be the results of hybridization and introgression of the FF population with parapatric Chlorocebus species, in contrast to the CF population, which was most likely not impacted by hybridization. Hybridization in the FF population was probably enhanced by an alteration of the bamboo forest habitat towards a more open woodland habitat, which enabled the parapatric Chlorocebus species to invade the Bale monkey's range and introgress the FF population. We therefore propose that the CF and FF Bale monkey populations should be managed as separate units when developing conservation strategies for this threatened species.

Highlights

  • Species with a restricted geographic distribution, and highly specialized habitat and dietary requirements, are vulnerable to extinction

  • Numts are highly unlikely to be present in our dataset, as we (1) used only faecal material in which nuclear DNA is largely degraded [76], (2) the hypervariable region I (HVI) region was amplified with genus- and mitochondrial DNA (mtDNA)-specific primers, and (3) no multiple peaks were obtained by direct sequencing of PCR products

  • One clade comprises all Bale monkey haplotypes from continuous forest (CF) and represents a sister lineage to a vervet haplotype (H23) from Sof Omar, whereas the second clade contains all haplotypes from fragmented forests (FF) Bale monkeys as well as from vervets, grivets and their putative hybrids

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Summary

Introduction

Species with a restricted geographic distribution, and highly specialized habitat and dietary requirements, are vulnerable to extinction. The effects of habitat alteration are detrimental to species with small geographic ranges and specialized niche requirements [2, 5, 9,10,11] One such species severely affected by habitat fragmentation is the Bale monkey (Chlorocebus djamdjamensis) [12, 13]. In addition to the Bale monkey, Ethiopia harbours two other native, but not endemic Chlorocebus species, the vervet (C. pygerythrus) and the grivet (C. aethiops) [16, 19,20,21] These two species are widely distributed, semi-terrestrial ecological generalists, inhabiting a variety of habitats and consuming a diverse diet of plant resources, invertebrates and small vertebrates [16, 22,23,24]. A phylogenetic study by Haus et al [20] revealed incongruences between mtDNA lineages and phenotypes in African green monkeys and suggested the occurrence of introgression between Bale monkeys and grivets as well as between vervets and grivets in Ethiopia

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